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Molecular Phylogenetics of Allodapine Bees, with Implications for the Evolution of Sociality and Progressive Rearing

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Molecular Phylogenetics of Allodapine Bees, with Implications for the Evolution of Sociality and Progressive Rearing Syst. Biol. 52(1):1–14, 2003 DOI: 10.1080/10635150390132632 Molecular Phylogenetics of Allodapine Bees, with Implications for the Evolution of Sociality and Progressive Rearing MICHAEL P. S CHWARZ,1 NICHOLAS J. BULL,1 AND STEVEN J. B. COOPER2 1School of Biological Sciences, Flinders University, G.P.O. Box 2100, Adelaide, South Australia 5001, Australia 2Evolutionary Biology Unit, South Australian Museum, Adelaide, South Australia 5000, Australia Abstract.—Allodapine bees have long been regarded as providing useful material for examining the origins of social behavior. Previous researchers have assumed that sociality arose within the Allodapini and have linked the evolution of sociality to a transition from mass provisioning to progressive provisioning of brood. Early phylogenetic studies of allodapines were based on morphological and life-history data, but critical aspects of these studies relied on small character sets, where the polarity and coding of characters is problematic. We used nucleotide sequence data from one nuclear and two mitochondrial gene fragments to examine phylogenetic structure among nine allodapine genera. Our data set comprised Downloaded from https://academic.oup.com/sysbio/article/52/1/1/1656919 by guest on 03 October 2021 1,506 nucleotide positions, of which 402 were parsimony informative. Maximum parsimony,log determinant, and maximum likelihood analyses produced highly similar phylogenetic topologies, and all analyses indicated that the tropical African genus Macrogalea was the sister group to all other allodapines. This finding conflicts with that of previous studies, in which Compsomelissa + Halterapis formed the most basal group. Changing the basal node of the Allodapini has major consequences for understanding evolution in this tribe. Our results cast doubt on the previous hypotheses that progressive provisioning and castelike social behavior evolved among lineages leading to the extant allodapine taxa. Instead, our results suggest that mass provisioning in Halterapis is a derived feature and that social behavior is an ancestral trait for all allodapine lineages. The forms of social behavior present in extant allodapines are likely to have resulted from a long evolutionary history, which may help explain the complexity of social traits found in many allodapine bees. [Allodapini; bees; phylogenetics; progressive rearing; social evolution.] Allodapine bees (family Apidae, tribe Allodapini) are concerns the evolution of progressive rearing from a most diverse and abundant in subsaharan Africa, but mass-provisioning ancestor and the consequences of this their distribution extends throughout the Old World scenario for social evolution (Michener, 1974, 1977, 1985, tropical and austral regions, northward into temperate 1990b). Asia Minor, and throughout the southern parts of this On the basis of morphological and brood-rearing region from India eastward (Michener, 1977). This tribe traits, Michener (1974, 1977) and Reyes (1998) suggested of bees is one of the most useful insect groups for exam- that Compsomelissa + Halterapis form the most basal allo- ining the evolution of social behavior because (1) social- dapine group. Halterapis mass provisions eggs once they ity varies widely among species and genera, allowing are laid, and Compsomelissa progressively rears young comparisons at multiple hierarchical levels, (2) there is larvae but mass provisions older larvae. Because bees substantial variation in demographic and ecological fea- in all other extant tribes in the Xylocopinae (Ceratinini, tures that are likely to affect selection on social traits, and Xylocopini, and Manueliini) are mass provisioners, it (3) many species are amenable to large-scale field experi- was thought that Halterapis and Compsomelissa repre- mentation, allowing statistical description of social and sented retention and partial retention, respectively, of a ecological traits (Schwarz et al., 1997, 1998). Allodapine plesiomorphic mass provisioning trait. This scenario is bees differ from all other bees in that for all genera other supported by the fact that in the Ceratinini (the sister than Halterapis, immatures are progressively and com- tribe to the Allodapini) most species remove cell parti- munally reared in undivided tunnels. This method of tions between immatures shortly before or after the pu- rearing leads to quite different selective factors under- pal moult, whereas in the more basal tribes (Manueliini lying sociality than are found for mass provisioning in- and Xylocopini), cell partitions are not removed at all sects (Michener, 1985). Progressive provisioning means or are removed by adults during pollen robbery or cell that immatures are dependent on the continued presence destruction involving nestmate conflict (Velthuis, 1987; of adults for food and protection, and communal rear- Blom and Velthuis, 1988; Hogendoorn and Velthuis, ing means that in multifemale colonies, parental care by 1995). Halterapis + Compsomelissa therefore seemed to mothers cannot be restricted to just their own daughters represent an intermediate stage between mass provision- but is spread to the entire brood within a nest (Schwarz, ing with late disruption of cell partitions, and complete 1988). progressive provisioning. The range in sociality among allodapines has lead In previous studies, the phylogenetic position of Hal- to much speculation on evolutionary transitions in so- terapis + Compsomelissa was based on only a few charac- cial behavior from a phylogenetic perspective. Neville ters, and one of these was the trait of mass provisioning et al. (1998) examined several life-history traits in the itself. However, the trait of mass provisioning as evi- Australian exoneurine genera (Exoneura, Exoneurella, dence for the basal position of Halterapis + Compsomelissa Brevineura, and the parasitic genus Inquilina), and Tierney in the Allodapini is problematic. In all Xylocopinae other et al. (2000) argued that a high level of phylogenetic than allodapines, pollen and nectar are accumulated and conservatism is present in the exoneurine genera for worked into a pollen ball before the egg is laid, whereas several life history traits. However, one of the most in all allodapines, eggs are laid first and then provided important phylogenetic hypotheses for allodapine bees with food. In all allodapines, pollen balls of various sizes 1 2 SYSTEMATIC BIOLOGY VOL. 52 can be provided to larvae and, in Allodapula, can even be TABLE 1. Taxa used in this study and their geographic origin. deposited on eggs (Michener, 1971). Thus, the kind of mass provisioning that occurs in Halterapis need not be Genus Species Collecting locality an intermediate stage between mass provisioning and Exoneura angophorae Dandenong Ranges, Victoria, Australia progressive provisioning, where the major evolutionary robusta Dandenong Ranges, Victoria, Australia Inquilina schwarzi Dandenong Ranges, Victoria, Australia change has simply been loss of cell partitions, but rather dawsoni Dandenong Ranges, Victoria, Australia may be a derived form of the provisioning patterns found Exoneurella tridentata Lake Gilles, South Australia, Australia in other allodapines. setosa Semaphore, South Australia, Australia Progressive provisioning in allodapines has been Brevineura xanthoclypeata Cobboboonee State Forest, Victoria, Australia viewed as an important factor in social evolution. ploratula Lake Gilles, South Australia, Australia Studies by Michener (1971) suggested that sociality in Allodape mucronata Kleinmond, Cape Province, + Halterapis Compsomelissa was either weakly developed South Africa Downloaded from https://academic.oup.com/sysbio/article/52/1/1/1656919 by guest on 03 October 2021 or only involved temporary predispersal assemblages. skaifeorum Kleinmond, Cape Province, In contrast, most other allodapines show more complex South Africa Braunsapis unicolor Lake Gilles, South Australia, Australia forms of sociality, suggesting that the evolution of social- protuberans Great Sandy National Park, ity may be associated with the transition from mass to Queensland, Australia progressive provisioning (Michener, 1985, 1990a). vitrea Soutpansberg Range, South Africa In this study, we used sequence data from one nu- paradoxa Cape St. Francis, Cape Province, South Africa clear and two mitochondrial gene fragments to exam- Compsomelissa borneri Meru National Park, Kenya ine phylogenetic relationships among several key allo- Halterapis nigrinervis Beaufort, Cape Province, South Africa dapine groups. Here, we discuss the implications of our Macrogalea candida Meru National Park, Kenya results for understanding the evolution of progressive zanzibarica Jambiani, Zanzibar Island, Tanzania provisioning and social behavior in these bees. Xylocopa bombylans Kangaroo Island, South Australia, (Lestis) Australia Manuelia postica Pucon, Chile Ceratina japonica Hokkaido, Japan METHODS (Neoceratina) Taxa Used We used 18 allodapine species from Africa and Doyle and Doyle’s (1990) CTAB method. Proteinase K Australia as our ingroup. We did not include repre- sentatives from the Allodapula clade (Michener, 1977) (10 l) was added to the solution prior to incubation at 55C for 2 hr with occasional mixing. DNA pellets because of problems with gene amplification, and we did not have representatives of the middle eastern genus were resuspended in 60 l of Millipore filtered ultrapure Exoneuridia (the nesting and social biology of this group (mq)H2O and stored frozen. A 1:5 dilution in mqH2Oof each DNA sample was used
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